Directory UMM :Data Elmu:jurnal:A:American Journal of Botany:Vol88.Issue1.Jan2001:

American Journal of Botany 88(1): 1–13. 2001.

INVITED SPECIAL PAPER

VESSELS

IN FERNS: STRUCTURAL, ECOLOGICAL, AND
EVOLUTIONARY SIGNIFICANCE1

SHERWIN CARLQUIST2

AND

EDWARD L. SCHNEIDER

Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, California 93105 USA
We have studied macerated xylem of ferns, supplemented by sections, by means of scanning electron microscopy (SEM) in a series
of 20 papers, the results of which are summarized and interpreted here. Studies were based mostly on macerations, but also on some
sections; these methods should be supplemented by other methods to confirm or modify the findings presented. Guidelines are cited
for our interpretations of features of pit membranes. Fern xylem offers many distinctive features: (1) presence of numerous vessels
and various numbers of tracheids in most species; (2) presence of vessels in both roots and rhizomes in virtually all species; (3)

presence of specialized end walls in vessels of only a few species; (4) multiple end-wall perforation plates in numerous species; (5)
lateral-wall perforation plates in numerous species; (6) porose pit membranes associated with perforation plates in all species; and (7)
pit dimorphism, yielding wide membrane-free perforations alternating with extremely narrow pits. Multiple end wall perforation plates
and lateral wall perforation plates are associated with the packing of tracheary elements in fascicles in ferns: facets of tips of elements
contact numerous facets of adjacent elements; all such contacts are potential sites for conduction by means of perforations. This
packing differs from that in primary xylem of dicotyledons and monocotyledons. Porosities in pit membranes represent a way of
interconnecting vessel elements within a rhizome or root. In addition, these porosities can interconnect rhizome vessel elements with
those of roots, a feature of importance because roots are adventitious in ferns as opposed to those of vascular plants with taproots.
Fully-formed or incipient (small-to-medium sized porosities in pit membranes) perforation plates are widespread in ferns. These are
believed to represent (1) ease of lysis of pit membranes via pectinase and cellulase; (2) numerous potential sites for perforation plate
formation because of fasciculate packing of tracheary elements; (3) evolution of ferns over a long period of time, so that lysis pathways
have had time to form; (4) lack of disadvantage in perforation plate presence, regardless of whether habitat moisture fluctuates markedly
or little, because ferns likely have maintaining integrity of water columns that override the embolism-confining advantage of tracheids.
Although all ferns share some common features, the diversity in xylem anatomy discovered thus far in ferns suggests that much
remains to be learned.
Key words: ecological anatomy; ferns; incipient perforation plates; intermittent perforation plates; lateral wall perforation plates;
multiple perforation plates; pit dimorphism; pit-membrane porosities; pit membrane remnants; vessel definitions; vessel evolution,
xylem.

Vessels were first reported for the ferns Nephrodium filixmas (L.) Schott and Pteridium aquilinum (L.) Kuhn by Russow (1873); vessel presence in Pteridium was confirmed by

Bliss (1939). Reports of vessels in ferns by Gwynne-Vaughan
(1908) were discounted by Bancroft (1911). However, distinctive vessels were reported in Marsilea (White, 1961), a report
confirmed by Loyal and Singh (1978). The possibility that
vessels might occur in other ferns was hinted by White (1962).
With light microscopy, White (1962) found end walls in tracheary elements of Astrolepis, Phlebodium, Polystichum, and
Woodsia that were distinct and suggestive of perforation
plates, but he could not demonstrate presence of perforations
with his methods. In deciding to use SEM to determine presence and nature of perforations, we began with these genera.
The usefulness of SEM in determining presence of pit membranes and pit membrane remnants has been demonstrated repeatedly in woody dicotyledons by Meylan and Butterfield
(1978) and by Carlquist (1992, 1997). We have investigated
vessels of monocotyledons with SEM and illustrated porose
pit membranes and pit membrane remnants (see Schneider and
Carlquist, 1998a, and Carlquist and Schneider, 1998a, and the
papers cited therein). When our earlier studies on fern tracheary elements revealed that the distinctive end walls cited by
1
2

White (1962) were, in fact, perforation plates (whereas lateral
walls of tracheary elements did show well-preserved pit membranes, we extended our studies to other genera and families.
We soon concluded that vessels might be much more widespread in ferns than had been suspected, and we also found a

series of structural features of interest in fern tracheary elements. The component papers in this series are listed below,
so that the numerous citations of species and genera can be
made without listing the relevant paper at each mention. The
occurrence of vessel elements or incipient vessel elements in
so many taxa might arouse skepticism in those who have not
had the opportunity to view a large number of preparations
such as ours. We have attempted to take into account any
possibilities of artifact formation. We have, however, offered
a discussion of preparation methods and interpretation below
in order to clarify the bases for our reports.
Bierhorst (1960) presented detailed light microscope studies
of tracheary elements of ferns. Not surprisingly, we have been
able to see a number of details not figured by Bierhorst. We
report, in a later section of this paper, some structures not
related to perforation plates that represent new reports in our
series.
In the process of surveying xylem in ferns, we searched for
correlations between tracheary element strucures and systematics or ecology. Although our sampling represents a small
proportion of fern species, the correlations are clear: the var-

Manuscript received 1 November 1999; revision accepted 2 June 2000.
Author for reprint requests.

1

2

AMERICAN JOURNAL

iables in structure are few, and therefore relatively easy to
interpret. We would like to offer data applicable to understanding of conductive physiology of ferns. However, very little is
known about conductive physiology in ferns. We hope that
our data on such features as presence of perforation plates on
lateral walls of tracheary elements, presence of multiple end
wall perforation plates, and highly porose or weblike pit membranes will be taken into account by those who pursue studies
on fern physiology.
New data on fern tracheary elements invite comparison with
data on xylem of other vascular plants. Such comparisons are
complicated by the diversity of opinion concerning the delimitations of ferns and the relationships of ferns (Hasebe et al.,
1995; Pryer, Smith, and Skog, 1995; Rothwell, 1996). We have

included Psilotaceae in our studies because some authors place
Psilotales in ferns (Hasebe et al., 1995), whereas others do not
(Rothwell, 1996). Comparisons between a group with primary
xylem only (living ferns) and groups with secondary growth
(cycads, gnetophytes) offer further interpretive concerns.
However, the similarities of tracheary elements among the fern
families in our studies outweigh the differences among the
families. Do these similarities reflect retention of ancient patterns of ferns (and other vascular plants, such as Selaginella:
Schneider and Carlquist, in press a, b)? Is this relative uniformity a reflection of growth forms and conductive physiology,
or is it a reflection of phylogenetic unity, or a combination of
both factors?
Major questions such as these are opened by our SEM studies. We wish to stress that our results are based on a small
sample. Also, our methods represent a limited range of techniques, and thus we emphasize the need for further studies,
especially those involving TEM and histochemistry.
DATABASE PAPERS
Our papers in order of writing, cited by species and family
or families are: Woodsia obtusa Spreng. ex Torr. (Dryopteridaceae or Woodsiaceae), [Carlquist, Schneider, and Yatskievych, 1997]; Pteridium aquilinum (L.) Kuhn (Pteridaceae) [Carlquist and Schneider, 1997a]; Phlebodium aureum (L.) Smith
(Polypodiaceae) and Polystichum acrostichoides (Mich.)
Schott (Aspidiaceae) [Schneider and Carlquist, 1997]; Astrolepis sinuata (Lag. ex Swartz) D. M. Benham & Windham
(Pteridaceae or Cheilanthaceae) [Carlquist and Schneider,

1997b]; Woodsia scopulina D. C. Eaton (Dryopteridaceae or
Woodsiaceae) [Schneider and Carlquist, 1998b]; Woodsia ilvensis (L.) R. Br. (Dryopteridaceae or Woodsiaceae) [Carlquist
and Schneider, 1998b]; Microgramma nitida A. R. Smith (Polypodiaceae) [Schneider and Carlquist, 1998c]; Platyzoma microphyllum R. Br. (Pteridaceae or Platyzomataceae) [Carlquist,
Schneider, and Kenneally, 1999]; Dicranopteris linearis
(Burm. f.) Underw. (Gleicheniaceae) [Schneider and Carlquist,
1998d]; Todea barbara (L.) Moore (Osmundaceae), Anemia
phyllitidis (L.) Moore and Lygodium flexuosum (L.) Swartz
(Schizaeaceae or Lygodiaceae) [Carlquist and Schneider,

OF

BOTANY

[Vol. 88

1998c]; Ophioglossum crotalophoroides Walt., O. pendulum
L., and O. vulgatum L. (Ophioglossaceae) [Schneider and Carlquist, 1999a]; Angiopteris evecta Hoffm., Danaea elliptica
Sm., D. wendlandii Reichenb. f., Macroglossum smithii (Racib.) D. H. Campbell, and Marattia fraxinea Sm. (Marattiaceae) [Carlquist and Schneider, 1999]; Nephrolepis exaltata
(L.) Schott (Davalliaceae) [Schneider and Carlquist, 1999b];
Ceratopteris thalictroides (L.) Brongn. (Parkeriaceae or Pteridaceae) [Carlquist and Schneider, 2000a]; Asplenium nidus L.

(Aspleniaceae), Elaphoglossum hirtum (Sw.) C. Christens.
(Elaphoglossaceae), and Vittaria lineata L. (Vittariaceae)
[Schneider and Carlquist, 1999c]; Alsophila australis R. Br.
(Cyatheaceae), Cibotium splendens (Gaud.) Kraj. ex Skottsb.
and Dicksonia antarctica Labill. (Dicksoniaceae), and Sadleria cyatheoides Kaulf. (Blechnaceae) [Carlquist, and Schneider,
2000b]; Psilotum nudum (L.) Griseb. and Tmesipteris obliqua
Chinnock (Psilotaceae) [Schneider and Carlquist, 2000a];
Bommeria hispida (Mett.) Underw., Cheilanthes californica
Hook., C. tomentosa Link, and Pellaea mucronata (D. C. Eaton) D. C. Eaton (Pteridaceae or Cheilanthaceae) [Carlquist
and Schneider, 2000c]; Marsilea drummondii Braun, M. quadrifolia L., and M. vestita Hook. & Grev. (Marsileaceae)
[Schneider and Carlquist, 2000b]; Callistopteris baldwinii (Eaton) Copel., Mecodium recurvum (Gaud.) Copel., and Vandenboschia davallioides (Gaud.) Copel. (Hymenophyllaceae)
[Carlquist, Schneider, and Lamoureux, 2000]. In listings of
genera below, the above sequence is followed.
INTERPRETIVE CRITERIA
Our studies are based mostly on macerations, but in the first
two papers of the series, sections were also employed. Our
methods are summarized in those two papers (Carlquist,
Schneider, and Yatskievych, 1997; Schneider and Carlquist,
1997a). Because pit membranes are sometimes thought to be
very delicate with relation to reagents and preparation methods, we have assembled a series of reasons, with citations of

earlier papers, that document why we believe our results are
reliable.
1) As observed by a wide variety of methods, pores develop
as a natural form of cell wall hydrolysis (achieved by pectinase
and cellulase) in particular pit membranes of particular species
(Butterfield and Meylan, 1982). The end product of this action
can be seen as perforations in vessels of dicotyledons and margos of pit membranes in coniferous tracheids. The result of
this lysis is a mesh of threads or, if the action of cellulase is
sufficient, removal of the entire pit membrane.
2) Different species of gymnosperms and angiosperms characteristically have pores of particular sizes in pit membranes
of tracheary elements; pores of these characteristic sizes are
observed despite the use of a variety of different methods of
preparation (Shane, McCully, and Canny, in press, Tables 2
and 3).
3) Although the data cited above are derived from gymnosperms and angiosperms, no worker has suggested that the
→

Figs. 1–7. Perforation plates of fern vessels with distinct end-wall perforation plates. Figs. 1–3. Woodsia ilvensis. 1. Perforation plate very similar in perforation
dimensions to lateral-wall pits. 2. Perforation plate with perforations wider axially and horizontally than lateral-wall pits. 3. Perforation plate markedly different
from lateral-wall pitting. Figs. 4–6. Pteridium aquilinum, perforation plates with relatively few bars. 4. Oblique perforation plate with slender bars, wide

perforations. 5. Near-transverse plate with slender bars. 6. Transverse plate with bars that fuse. 7. Marsilea quadrifolia, perforation plate with one bar. Scales
5 10 mm in all figures.

January 2001]

CARLQUIST

AND

SCHNEIDER—EVOLUTION

OF VESSELS IN FERNS

3

4

AMERICAN JOURNAL

same kinds of porose pit membranes observed in ferns and

Selaginella (Schneider and Carlquist, in press a, b) are artifacts
of reagents or preparation methods in ferns but not in the dicotyledons and monocotyledons where they have been reported (Carlquist, 1992, 1997; Carlquist and Schneider, 1998a;
Meylan and Butterfield, 1978; Schneider and Carlquist,
1998a).
4) Where end wall perforation plates of fern tracheary elements are different from lateral walls (by virtue of different
patterns in the underlying secondary wall framework), the end
wall perforation plates lack pit membranes while the lateral
walls possess them in Woodsia (e.g., Fig. 1–3, 17). If maceration techniques or drying techniques were responsible for removal of pit membranes in the end wall perforation plates of
Woodsia spp., the pit membranes should be removed from
lateral walls as well, and pit membranes should be removed
in a random fashion in tracheary elements in ferns at large.
Absence of pit membranes, except in instances we have been
able to attribute to handling, is not at all random in pits (or
perforations) of the fern tracheary elements we examined. The
absence of random removal of pit membranes seems to us very
strong evidence for believing that our methods have produced
essentially accurate images.
5) Facets lacking pit membranes are adjacent to facets with
intact pit membranes in many cases we have observed (Fig.
10). The marked difference in pit membrane conditions in facets adjacent to each other does not support interpretation of

membrane absence as an artifact.
6) In the first two papers of our series (Carlquist, Schneider,
and Yatskievych, 1997; Schneider and Carlquist, 1997) we
used both macerated and sectioned materials, and obtained the
same results with both techniques.
7) In vessel elements in which the size and morphology of
the perforations are like the lateral wall pits, upper and lower
ends of perforation plates (as well as incipient perforation
plates) often bear porose pit membranes. The porose pit membranes indicate a transition between lateral wall pitting and
perforations. In Fig. 16, porose pit membranes of such a transitional area are shown at left, adjacent to a facet with intact
pit membranes at right. The distribution of porose pit membranes (in comparison to distribution of non-porose pit membranes) is not random in our preparations.
8) We generally have not illustrated torn or ripped pit membranes in our papers. However, torn pit membranes or areas
of pit membranes were present in our preparations and were
readily recognized as such. Torn membranes contrast clearly
with the pores and holes in pit membranes because the pores
have smooth outlines, whereas artifacts produced by tearing
have irregular edges (Fig. 21).
9) Tracheids with intact pit membranes and a narrow shape
(Fig. 15) coexist with vessel elements that are wider and have
perforation plates on end walls in Ceratopteris (Fig. 14, 15)
and Alsophila (Fig. 22). If preparation methods could artificially produce perforation plates, narrower tracheids covered

OF

BOTANY

[Vol. 88

with unaltered pits as well as vessel elements (wider than the
tracheids) with facets bearing intact pit membranes would not
be expected in preparations such as ours.
10) Striate pit membranes (Figs. 16, 22) represent artifacts,
in our opinion. We believe that the action of the SEM electron
beam results in this appearance or at the least exaggerates it.
We have considered all appearances related to striate nature of
pit membranes as potential artifacts. Uneven thickness in pit
membranes resulting in weblike appearances, however, is interpreted as natural.
11) We believe that air drying of cells does not produce the
porosities or weblike appearances of pit membranes. When a
wide range of methods is used to demonstrate presence or
absence of pores (including introduction of particles of known
diameters into the conductive stream), porosity size is not related to preparation method, but rather characterizes particular
species (Shane, McCully, and Canny, in press, Tables 2 and
3). More significantly, students of xylem have repeatedly reported cavitation of xylem cells in the living plant. Ferns have
not been studied in this respect, but can be assumed to experience replacement of water by air in tracheary elements under
stress conditions but inevitably by age also. Therefore, pit
membranes of air-filled tracheary elements have been subjected to air drying in the living plant. To rehydrate such elements
in a pickling solution and then apply critical point drying to
such cells would be superfluous and illogical. If porose pit
membranes were the result of air drying, the extensive areas
of intact nonporose membranes on facets adjacent to membranes with porose membranes would be inexplicable.
12) Our results are entirely compatible with results obtained
thus far with other methods by other workers. For example,
Morrow and Dute (1998, 1999) did not find pores in pit membranes in Botrychium using transmission electron microscopy,
nor did we with SEM (unpublished data).
13) We have avoided use of stem or root portions that could
contain meristematic or differentiating cells. Therefore, the
presence or absence of pit membranes cannot be attributed, in
our preparations, to different degrees of maturation of cells.
14) We did not attempt to control for age of tracheary elements (as indicated by distance from an apical meristem, for
example), although we used liquid-preserved portions of living
plants. Therefore, in any given preparation, some of the tracheary elements might have been inactive ones while others
were actively conducting elements. We did not observe differences among tracheary elements, within a preparation.
While conceivably bacterial or fungal action might remove pit
membranes from inactive tracheary elements, this is unlikely
to account for the patterns we observed, and no evidence for
such deterioration of fern tracheary elements has been presented in studies we know. Duerden (1934) claimed vessels
with simple perforation plates (but with pit membranes on lateral walls) in homophyllous species of Selaginella. Duerden’s
(1934) studies have never been questioned, despite the fact
→

Figs. 8–12. Perforations that are not arranged in a single scalariform perforation plate per end wall. Figs. 8–9. Microgramma nitida. 8. All facets at element
tip are perforation plates. 9. Facets that are perforation plates, showing pit dimorphism (alternating wide and narrow perforations). 10. Vandenboschia davallioides. Facets, from left to right, that illustrate perforations formed in relation to pit dimorphism, a lateral wall of intact pit membranes, and a portion of a
scalariform perforation plate. Figs. 11–12. Bommeria hispida. Facets that show aspects of pit dimorphism. 11. Five perforations alternating with groups of very
narrow pits; other facets in the photograph show intact lateral-wall pitting. 12. Portion of facet with pit dimorphism; membranes of narrow pits, upper left, are
porose. Scales 5 10 mm in Figs. 8–11; scale 5 5 mm in Fig. 12.

January 2001]

CARLQUIST

AND

SCHNEIDER—EVOLUTION

OF VESSELS IN FERNS

5

6

AMERICAN JOURNAL

that they were based on herbarium species and the preparation
method involved only maceration techniques.
CHARACTERISTICS OF FERN TRACHEARY
ELEMENTS
Vessel elements with distinctive perforation plates—The
perforation plates of Figs. 1–7 are arranged from those that
show progressively greater degrees of simplification of the
perforation plates. In all of these, however, the perforation
plates are end walls that lack pit membranes, whereas the lateral wall pits contain pit membranes. The first three in this
sequence (Figs. 1–3), from Woodsia ilvensis, show long perforation plates with perforations little if at all larger than lateral
wall pits in the first (Fig. 1), but in Fig. 2, we see perforation
size detectably different from lateral wall pit size. In Fig. 3,
the perforations are markedly larger than the lateral wall pits.
A continuation of this series is shown in Figs. 4–6, Pteridium
aquilinum. The bars of the perforation plates in Fig. 4 are
slender and probably lack borders; the plate is oblique. More
nearly transverse plates are represented in Figs. 5 and 6. The
perforation plate of Fig. 5 has few and slender bars; that of
Fig. 6 has bars that fuse as they traverse the plate. A single
bar across a perforation plate is shown for Marsilea in Fig. 7.
The ultimate reduction would be represented by a simple perforation and some simple perforation plates are reported for
Marsilea by White (1961, 1962).
A moderate degree of differentiation between perforation
plates and lateral wall pitting was also observed in Astrolepis
sinuata, Polystichum acrostichoides and Woodsia scopulina.
Ferns not mentioned in this and the preceding paragraph were
not observed to have secondary wall frameworks for perforation plates that differed from those of the lateral wall pitting.
Multiple end-wall perforation plates—Reduction in number of bars in perforation plates, described in the preceding
section, has been considered an indicator of phylogenetic specialization in angiosperms. Most ferns, however, do not exemplify this trend and have vessel elements with end walls
that resemble lateral walls (Fig. 13). However, multiple endwall perforation plates, a feature rarely reported in other vascular plants, were observable in a number of fern tracheary
elements.
Multiple perforation plates per vessel element tip are illustrated here by Microgramma (Figs. 8, 9). In the element tip
of Fig. 8, the three facets shown lack pit membranes. The
vessel element portion shown in Fig. 9 illustrates absence of
pit membranes in all facets, both those of the facing facets and
those on the back facets. We have figured the occurrence of
several perforation plate facets per tracheary element tip in
Polystichum acrostichoides, Woodsia scopulina, Platyzoma
microphyllum, Dicranopteris linearis, Todea barbara,
Ophioglossum pendulum, O. vulgatum, Danaea wendlandii,
Macroglossum smithii, Marattia fraxinea, Nephrolepis exal-

OF

BOTANY

[Vol. 88

tata, Elaphoglossum hirtum, Sadleria splendens, Alsophila
australis, Dicksonia antarctica, Cheilanthes californica, Marsilea spp., Callistopteris baldwinii, and Vandenboschia davallioides. However, multiple perforation plates are probably
more widespread in ferns than our reports presently indicate.
The occurrence of multiple end-wall perforation plates on tracheary elements can be correlated with the arrangement (packing) of tracheary elements in ferns, as discussed later.
Pit dimorphism—Pit dimorphism that results in the formation of wide perforations alternating with one or more narrow intervening pits is illustrated here for Microgramma nitida
(Fig. 9), Vandenboschia davallioides (Fig. 10), and Bommeria
hispida (Figs. 11, 12). Similar pit dimorphism resulting in formation of perforations interspersed with pits on a wall was
figured by us in Phlebodium aureum, Polystichum acrostichoides, Platyzoma microphyllum, Dicranopteris linearis,
Anemia phyllitidis, Ophioglossum pendulum, Danaea elliptica,
D. wendlandii, Psilotum nudum, and Cheilanthes californica.
Wide pits (possibly perforations) alternating with narrow pits
were figured by Bierhorst (1960) for Angiopteris evecta
Hoffm., Asplenium viride Huds., and Osmunda cinnamomea
L. Bierhorst’s work was based on light microscopy, so he
could not have readily observed absence of pit membranes in
the wide pits, and thus his lack of comment on this phenomenon is understandable.
Lateral-wall perforation plates—In macerations of some
ferns, lateral walls are not readily distinguished from end
walls. This is not true in Pteridium, in which lateral walls are
easily distinguished from the end wall perforation plates. In
our Pteridium study (Carlquist and Schneider, 1997, Figs. 11–
13), we showed areas of lateral wall pits in which pores are
so large that one should likely say that the pits have become
converted into perforations, and therefore, lateral-wall perforation plates are present. These lateral wall perforation plates
are readily distinguished from the end-wall perforation plates
of Pteridium, which have fewer, narrower bars intervening between wide perforations, and no pit membrane remnants in the
perforations. In the present paper, lateral-wall perforation
plates are illustrated for Woodsia obtusa (Fig. 7), in which
porose pit membranes are present, and Ceratopteris thalictroides (Fig. 18), in which relatively large holes are present.
Intermittent perforation plates—The lateral-wall perforation plate figured for Ceratopteris thalictroides (Fig. 18) is
subdivided by intact pits, and is thus an intermittent perforation plate. We observed such intermittent perforation plates in
other ferns as well. By definition, pit dimorphism in which the
wide pits are perforations results in intermittent perforation
plates.
At left in Fig. 16 is a lateral-wall facet with porose pit membranes; this facet therefore constitutes an incipient lateral wall
perforation plate.
→

Figs. 13–18. Tracheary elements of Ceratopteris thalictroides (Figs. 13–16, 18) and Woodsia obtusa (Fig. 17). 13. End-wall perforation plate that extends
about two-thirds of the length of the photograph, showing similarity between perforation plate and lateral-wall pitting. 14. Typical short vessel element of C.
thalictroides, with a distinct end-wall perforation plate (above). 15. Slender tracheary element on which no perforations are visible, and which therefore is
interpreted as a tracheid. 16. Adjacent facets from a single tracheary element; facet at left contains pits with porose membranes, whereas facet at right contains
pits with nonporose membranes. 17. Portion of lateral-wall perforation plate, to show pores of various sizes in the pit membranes. 18. Lateral-wall perforation
plate in which perforations take the form of elongated ellipses; this perforation plate is intermittent, with intact pits between groups of perforations. Scales 5
10 mm in Figs. 13–15 scales 5 5 mm in Figs. 16–18.

January 2001]

CARLQUIST

AND

SCHNEIDER—EVOLUTION

OF VESSELS IN FERNS

7

8

AMERICAN JOURNAL

We could identify perforations as present on lateral walls in
some tracheary elements. However, in our preparations, wall
facets are very long and few elements are isolated well enough
and intact enough to designate all facets either as end walls
or as lateral walls. Thus, certain identification of lateral wall
perforation plates in all cases was not possible.
Vessel elements and tracheids—In Ceratopteris thalictroides, the shortness of tracheary elements and the success of
macerations permitted us to see isolated tracheary elements
well. Some of these elements were wider and shorter and had
perforation plates on end walls and thus were clearly vessel
elements (Fig. 14). Other tracheary elements in this species
were narrower, and end walls were revealed with sufficient
clarity, so that we could reasonably identify them as tracheids
(Fig. 15). In other ferns, we were rarely able to make this
distinction. Because the SEM method can only reveal the surfaces facing away from the mount, there is always some degree of doubt about whether a facet hidden from view contains
perforations or not. Nevertheless, we can generalize, based on
the abundance of perforation plates observed in our preparations, that in the xylem of ferns we studied, tracheids were
few or none. Prior to our studies, vessel elements were assumed to be absent in most ferns. In the ferns in which vessels
had been reported (e.g., Pteridium), earlier authors did not
present analyses of whether tracheids were also present (e.g.,
Bliss, 1939). Thus, no study prior to our work on Ceratopteris
presented the likelihood that vessel elements could coexist
with tracheids in fern xylem. Further work, perhaps with particles of various sizes introduced into actively conducting xylem, needs to be done to confirm the idea that fern xylem can
consist mostly or wholly of vessel elements.
Porose pit membranes and incipient perforation plates—
Porose pit membranes (Figs. 19, 20) were observed in all of
our studies, cited above. The modes of occurrence of these
pores are as follows: (1) throughout incipient perforation
plates (usually lateral wall perforation plates, Fig. 16, left); (2)
at upper and lower ends of perforation plates, where the porose
pits form a transition between perforations and intact pits; (3)
in narrow pits, where accompanied by wide pits in instances
of pit dimorphism (Fig. 12, upper left).
Modifications of porose pit membranes in the direction of
enlargement of pores are common. These modifications include: (1) occurrence of one to several large holes as well as
porose membranes, forming an incipient perforation (Figs. 17,
20, 22) or else presence of large holes without porose pit membranes (Fig. 18); (2) threadlike or weblike pit membrane remnants (Fig. 21), which may or may not include porose segments.
Most of the facets we examined, however, possess intact pit
membranes (Fig. 23) in which pores, if present, were so minute that they were beyond the resolving ability of our equipment and which probably would be referable to the category
of plasmodesmata rather than pores.

OF

BOTANY

[Vol. 88

Other newly reported structural details—During the course
of our studies to determine presence of vessel elements in the
ferns we studied, we encountered a number of noteworthy
structures.
1) Tracheary elements that are short and have numerous
short facets (Fig. 23). These were observed only in Cyatheaceae.
2) Grooves interconnecting pit apertures (Fig. 24). These
were observed only on the inner surfaces of vessels of Pteridium aquilinum. Such grooves may be more widespread in
ferns, but we viewed the inner surfaces of vessels only in our
first two fern studies in which sections of tracheary elements
were prepared and observed. Such grooves (also termed ‘‘coalescent pit apertures’’) are widespread in dicotyledons, but
our report is apparently the first in ferns.
3) Cushions of wall material present at facet edges of tracheary elements. We observed these in Danaea elliptica (Figs.
25, 26) and Elaphoglossum hirtum (Fig. 27), two ferns that
are not at all closely related. We know of no previous report
of such structures prior to ours.
4) In Vandenboschia davallioides (Fig. 28), Dicranopteris
linearis, and Anemia phyllitidis we observed that at facet edges, the horizontal secondary wall framework segments terminate. Thus, the secondary wall framework consists of transverse bars with widened ends, and the facet angle therefore
consists of primary wall separating the ends of these barlike
structures. Ordinarily, a secondary wall framework that forms
a continuous skeleton for the tracheary element is illustrated
for fern metaxylem, and a vertical (axial) ridge of secondary
wall material, rather than an absence of secondary wall material, is characteristic of tracheary elements of most ferns.
5) We examined roots and stems (rhizomes) of all ferns we
studied (the axis of Psilotaceae is not differentiated into roots
and stems, however). In all species for which we had both root
and stem material that yielded good results, vessel elements
were observed in both roots and stems.
FERN TRACHEARY ELEMENTS: NEW
INTERPRETATIONS
1) Vessel elements with a distinctive end wall perforation
plate at either end characterize angiosperms. Angiosperm vessels, with few exceptions, are thought to be like superposed
pipe segments, and lateral contacts between vessels bear pits
rather than perforations. This type of end-wall perforation
plate does occur in ferns that have end walls different from
lateral walls (wide perforations between narrow bars in the
perforation plates), such as Pteridium or Woodsia (Figs. 1–6).
However, even in these fern genera, lateral wall perforation
plates, less specialized than those on end walls, occur. This
may relate to the packing of tracheary elements in ferns (Figs.
29, 30). Because tracheary elements occur in fascicles in fern
steles, there are numerous lateral-wall contacts on which perforation plates can develop (Fig. 29). In Pteridium (Fig. 30),
parenchyma intrudes into the xylem and subdivides it into segments of fewer vessels each. This situation resembles the pri-

→
Figs. 19–22. Tracheary elements of Hymenophyllaceae (Figs. 19, 21), Dicksoniaceae (Fig. 20), and Cyatheaceae (Figs. 22, 23). Figs. 19–20. Porose pit
membranes of incipient perforation plates. 19. Callistopteris baldwinii, two pits. 20. Dicksonia antarctica, three pits. 21. Perforations in which pit membrane
remnants form threadlike or weblike configurations. Figs. 22–23. Alsophila australis. 22. Perforation-plate facet in which each pit has a porose membrane with
a single, large central hole. 23. Tip of tracheary element with short facets with intact pits. Scales 5 5 mm in Figs. 19–22; scale 5 1 cm in Fig. 23.

January 2001]

CARLQUIST

AND

SCHNEIDER—EVOLUTION

OF VESSELS IN FERNS

9

10

AMERICAN JOURNAL

OF

BOTANY

[Vol. 88

January 2001]

CARLQUIST

AND

SCHNEIDER—EVOLUTION

mary xylem of angiosperms, in which rows of vessels are separated from each other and therefore lateral-vessel contacts are
relatively few. Ferns with little lateral contact among tracheary
elements might be expected to show prominent end-wall perforation plates, as is the case in Pteridium and Woodsia.
2) Most ferns, in contrast with Pteridium and Woodsia, have
perforation plates that are not different from lateral-wall pitting
with respect to the secondary-wall framework of the end wall.
The only difference is in the absence of pit membranes in the
perforations. Although angiosperms show specialization of
end-wall perforation plates in most genera, no such modifications are present in most fern genera. Perhaps the reason
why ferns have perforation plates yet retain unspecialized
structure in them is that there is a multiplicity of perforation
plates on fern tracheary elements and that most ferns do not
have the selective pressure for rapid rates of conduction that
angiosperms experience.
3) Most ferns have multiple end-wall facets that are converted into perforation plates by lysis of pit membranes (Fig.
8), rather than single perforation plates per end wall. These
multiple perforation-plate facets are likely related to packing
of metaxylem elements (Fig. 28). The end of a given tracheary
element is not in contact with the end wall of a single superposed element at either end, but with side walls of a multiplicity of elements. The multiple contacts among tracheary
elements in most ferns may predispose the tracheary elements
to develop both lateral-wall and end-wall perforation plates,
as suggested under (1) above. Tracheary elements in ferns are
often very long, and the differentiation into end-wall and lateral-wall facets is minimal.
4) The occurrence in ferns of both end-wall and lateral-wall
perforation plates has the effect of converting a fascicle of
tracheary elements into a kind of aggregate vessel. No part of
such a fascicle of elements is isolated from any other part in
terms of conduction. Fascicles of vessel elements interconnected with each other by lateral perforation plates as well as
end-wall perforation plates have not been reported in other
groups of vascular plants except Selaginella, depending on
definition of lateral-wall perforation plate (Schneider and Carlquist, in press a, b).
5) A series of wide perforations alternating with narrow pits,
a condition that we are terming ‘‘pit dimorphism,’’ has a potential effect on the conductive stream of a scalariform perforation plate. Evidently ferns have been able to develop these
vicarious perforation plates by means of pit dimorphism more
successfully than have other vascular plants, because we know
of no reports of pit dimorphism resulting in perforation-plate
equivalents in groups other than ferns except for Selaginella
(Schneider and Carlquist, in press a, b).
6) Porose pit membranes that range from incipient perforation plates (where pores are small) to perforation plates in
which the pores in pit membranes open large portions of a pit
membrane to the conductive stream, are common in ferns. The
existence of this range of perforation plates has not, hitherto,
been reported in other groups of vascular plants, except for

OF VESSELS IN FERNS

11

recent instances such as our studies of vessels of monocotyledons (e.g., Carlquist and Schneider, 1998a; Schneider and
Carlquist, 1998a) and Selaginella (Schneider and Carlquist, in
press a, b).
7) The occurrence in ferns of numerous incipient perforation
plates or of perforation plates with appreciable areas of pit
membrane remnants in perforations raises the question of terminology with respect to vessel elements. When are pit membranes provided with pores of such size and abundance that
one must say perforations (and therefore vessel elements) are
present? By using the term incipient perforation plate, we recognize a transition, even if we do not define a distinction between tracheids and vessel elements in such transitional instances. One might use quantitative criteria, such as the ability
to transmit microspheres of known diameters from one tracheary element to another. Even this definition would likely
be arbitrary. One notes the capability of margo pores in conifer
tracheids to allow passage of relatively large particles in comparison to porosities in pit membranes of tracheary elements
of other vascular plants (Shane, McCully, and Canny, in
press), yet undoubtedly this information would not lead anatomists to question the presence of tracheids in conifers. As a
working definition, we have tended to regard presence of porosities totalling ø50% of the area of a pit membrane or more
as constituting a perforation. However, such criteria as passage
of air bubbles of minimal size or other physiological criteria
are needed: terminology of tracheary elements should reflect
functional distinctions, if possible.
8) Porosities in pit membranes offer a potential method of
interconnection between tracheary elements that are in contact
but which have no intercontinuous ontogenetic relationship
with each other. A prime example of this is the interconnection
of vessels in adventitious roots with the vessels of the stem
on which the adventitious roots form. The possible function
of porosities in pit membranes to form a pathway for the conductive stream is important, because if vessels occur in both
stems and roots of ferns (see above) and monocotyledons (Carlquist and Schneider, 1998a, and earlier papers in that series),
such a mechanism for facilitating conduction between root and
stem vessels is of selective value. Such a possible function has
been mentioned in maize by Shane, McCully, and Canny (in
press), and is equally applicable to ferns.
9) In those ferns with end-wall perforation plates that differ
in framework from lateral-wall pitting (or lateral-wall perforation plates), the simplification of the perforation plate is related to ecology. Marsilea, Pteridium, and Woodsia, which
exemplify this, live in situations with marked fluctuation in
water availability and show trends to fewer bars associated
with wider perforations. However, other ferns occur in ecological regimes in which drying or freezing of soil offers extremes as severe as those experienced by those three genera,
yet these other ferns (e. g., Cheilanthes, Pellaea, Platyzoma)
do not have such modifications of the secondary-wall framework of perforation plates. These latter genera do, however,
have other means other than simplified perforation plates by

←
Figs. 24–27. Unusual structural details of fern tracheary elements from sections (Fig. 24) and macerations (Figs. 25–27). 24. Pteridium aquilinum, inner
surface of vessel from section, showing elliptical grooves interconnecting two or three pits (at right). Figs. 25–26. Danaea elliptica, portions of facet edge
viewed obliquely. 25. Cushionlike structures at facet edges of adjacent tracheary elements. 26. Cushionlike structures adjacent to pits, in face view. 27.
Elaphoglossum hirtum. Facet of tracheary element (center) on either side of which cushionlike structures are present. 28. Vandenboschia davallioides. Edge
between two facets. The secondary wall is absent from elliptical portions of the facet edge. Scales 5 10 mm in Figs. 24–25; scales 5 5 mm in Figs. 26–28.

12

AMERICAN JOURNAL

OF

BOTANY

[Vol. 88

Figs. 29–30. Transections of tracheary elements from rhizomes, as seen with light microscopy. 29. Osmunda cinnamomea. Tracheary elements not intermixed
with parenchyma cells. 30. Pteridium aquilinum. Bands of parenchyma separate groups of two to several tracheary elements. Scale for both figures above Fig.
29 (divisions 5 10 mm).

which the conductive stream potentially can be facilitated during brief periods of water availability. Such means include
multiple end wall perforation plates, lateral-wall perforation
plates, and perforations that result from pit dimorphism. In
angiosperms, degree of simplification of perforation plate is
closely keyed to degree of fluctuation in water availability
(Carlquist, 1975). Enhancement of the conductive capabilities
of a vessel of an angiosperm must be accomplished by modification of the end wall, because the variety of perforation
plates and perforation-plate substitutes present in ferns are not
available in angiosperms.
10) Vessels are much more common in ferns than hitherto
supposed. Because many ferns that have perforation plates occur in habitats with relatively uniformly moist environments
(e.g., Marattiaceae), strong fluctuation in moisture availability
cannot be hypothesized as a requirement to explain vessel origin in ferns. Lysis of pit membranes by pectinase and cellulase is apparently not a complicated process (Butterfield and
Meylan, 1982). If this is true, vessels could be expected to
develop independently in a number of clades of vascular
plants. Once large porosities are formed, removal of most or
all of the pit membrane remnants is all but inevitable. Special
mechanisms (e.g., fibrils separating large pores in margos of
pits of conifer tracheids) that do not follow this pattern but
represent alternative mechanisms for enhancement of conduction exist. Perforation plates (or equivalent structural enhancements of conductive capability) are not known to be of any

detriment in mesic situations. For example, dicotyledons of
bogs show no fewer simple perforation plates than do plants
of noninundated areas (Carlquist, unpublished data). The potential role of imperforate tracheary elements in deterring
spread of air embolisms has often been cited, and undoubtedly
does occur. However, mechanisms for control of transpiration
may override the potential advantages of tracheids in increasing safety and integrity of the water columns of a plant from
spread of air bubbles. For example, Gates (1968) measured a
diffusive resistance in Pteridium higher than that of any other
vascular plant he studied.
In summarizing our data, we wish to emphasize that our
survey, although it covers all major families of ferns, is based
on limited material when one considers the large number of
fern species in existence. The opportunities for research in
structure of fern tracheary elements by means of electron microscopy are extensive. Moreover, we hope that plant physiologists will become interested in studying vascular plants
such as ferns that offer a range of conductive pathways not
present in angiosperms or gymnosperms.
LITERATURE CITED
BANCROFT, N., 1911. On the xylem elements of the Pteridophyta. Annals of
Botany 25: 746–759.
BIERHORST, D. W., 1960. Observations on tracheary elements. Phytomorphology 10: 249–305.

January 2001]

CARLQUIST

AND

SCHNEIDER—EVOLUTION

BLISS, M. C., 1939. The tracheal elements in the ferns. American Journal of
Botany 26: 620–624.
BUTTERFIELD, B. G., AND B. A. MEYLAN. 1982. Cell wall hydrolysis in the
tracheary elements of the secondary xylem. In P. Baas [ed.], New perspectives in wood anatomy, 71–84. Dr. Martinus Nijhoff/Dr. W. Junk,
The Hague, The Netherlands.
CARLQUIST, S., 1975. Ecological strategies of xylem evolution. University
of California Press, Berkeley, California, USA.
———. 1992. Pit membrane remnants in perforation plates of primitive dicotyledons and their significance. American Journal of Botany 79: 666–
672.
———. 1997. Pentaphragma: a unique wood and its significance. IAWA
Journal 18: 3–12.
———, AND E. L. SCHNEIDER. 1997a. SEM studies on vessels in ferns. 2.
Pteridium. American Journal of Botany 84: 581–587.
———, AND ———. 1997b. SEM studies on vessels in ferns. 4. Astrolepis.
American Fern Journal 87: 43–50.
———, AND ———. 1998a. Origin and nature of vessels in monocotyledons. 5. Araceae subfamily Colocasioideae. Botanical Journal of the Linnean Society 128: 71–86.
———, AND ———. 1998b. SEM studies on vessels in ferns. 6. Woodsia
ilvensis, with comments on vessel origin in ferns. Flora 193: 179–185.
———, AND ———. 1998c. SEM studies on vessels in ferns. 10. Selected
Osmundaceae and Schizaeaceae. International Journal of Plant Sciences
159: 788–797.
———, AND ———. 1999. 12. Marattiaceae, with comments on vessel patterns in eusporangiate ferns. American Journal of Botany 86: 457–464.
———, AND ———. 2000a. SEM studies of vessels in ferns. 14. Ceratopteris. Aquatic Botany 66: 1–8.
———, AND ———. 2000b. SEM studies of vessels in ferns. 16. Pacific
tree ferns (Blechnaceae, Cyatheaceae, Dicksoniaceae). Pacific Science
54: 75–86.
———, AND ———. 2000c. SEM studies of vessels in ferns. 18. Montane
cheilanthoid ferns (Pteridaceae) of North America. Aliso 19: 31–39.
———, ———, AND K. F. KENNEALLY. 1999. SEM studies on vessels in
ferns. 8. Platyzoma. Australian Journal of Botany 47: 277–282.
———, ———, AND C. LAMOUREUX. 2000. SEM studies on vessels in
ferns. 20. Hawaiian Hymenophyllaceae. Pacific Science 54: 365–375.
———, ———, AND G. YATSKIEVYCH. 1997. SEM studies on vessels in
ferns. 1. Woodsia obtusa. American Fern Journal 87: 1–8.
GATES, D. M., 1968. Transpiration and leaf temperature. Annual Review of
Plant Physiology 19: 211–238.
GWYNNE-VAUGHAN, D. T., 1908. On the real nature of the tracheae in the
ferns. Annals of Botany 22: 517–523.
HASEBE, M., P. G. WOLF, K. M., PRYER, K. UEDA, M. ITO, R. SANO, G. J.
GASTONY, J. R. MANHART, N. MURAKAMI, E. H. CRANE, C. H. HAUFLER, AND W. D. HAUK. 1995. Fern phylogeny based on rbcL sequences. American Fern Journal 85: 134–181.
LOYAL, D. S., AND L. SINGH. 1978. A further investigation of the morphology of vessels in Marsilea. Proceedings of the Indian Academy of Sciences (Plant Sciences—4) 87B: 335–346.
MEYLAN, B. A., AND B. G. BUTTERFIELD. 1978. The structure of New Zea-

OF VESSELS IN FERNS

13

land woods. DSIR Bulletin 222. New Zealand Department of Scientific
and Industrial Research, Wellington, New Zealand.
MORROW, A. C., AND R. R. DUTE. 1998. Development of the torus-bearing
pit membrane in Botrychium dissectum. IAWA Journal 19: 429–441.
———, AND ———. 1999. Electron microscopic investigation of the coating
found on torus-bearing pit membranes of Botrychium dissectum, the common grape fern. IAWA Journal 20: 359–373.
PRYER, K., A. R. SMITH, AND J. E. SKOG. 1995. Phylogenetic relationships
of extant ferns based on evidence from morphology and rbcL serquences.
American Fern Journal 85: 205–262.
ROTHWELL, G. W., 1996. Phylogenetic relationships of ferns: a palaeobotanical perspective. In J. M. Camus, M. Gibby, and R. J. Johns [eds.], Pteridology in perspective, 395–404. Royal Botanic Gardens, Kew, Richmond, Surrey, UK.
RUSSOW, E. 1873. Vergleichende Untersuchungen betreffend die Histologie
(Histographie und Histogenie) der vegetativen und sporenbildenen Organe und die Entwicklung der Sporen der Leitbundel-Kryptogamen, mit
Berücksichtigung der Histologie der Phanerogamen, ausgehend von der
Betrachtung der Marsiliaceen. St. Petersburg Academy of Sciences Memoirs, Series 7, 19(1): 1–207.
SCHNEIDER, E. L., AND S. CARLQUIST. 1997. SEM studies on vessels in ferns.
3. Phlebodium and Polystichum. International Journal of Plant Sciences
1158: 343–349.
———, AND ———. 1998a. Origin and nature of vessels in monocotyledons. 4. Araceae subfamily Philodendroideae. Journal of the Torrey Botanical Society 125: 253–260.
———, AND ———. 1998b. SEM studies on vessels in ferns. 5. Woodsia
scopulina. American Fern Journal 88: 17–23.
———, AND ———. 1998c. SEM studies on vessels in ferns. 7. Microgramma nitida. Anales del Instituto Biologico de la Unversidad Autonomica de México 69: 1–7.
———,